Spatial population expansion promotes the evolution of cooperation in an experimental Prisoner's Dilemma.

Abstract

Cooperation is ubiquitous in nature, but explaining its existence remains a central interdisciplinary challenge. Cooperation is most difficult to explain in the Prisoner's Dilemma game, where cooperators always lose in direct competition with defectors despite increasing mean fitness. Here we demonstrate how spatial population expansion, a widespread natural phenomenon, promotes the evolution of cooperation. We engineer an experimental Prisoner's Dilemma game in the budding yeast Saccharomyces cerevisiae to show that, despite losing to defectors in nonexpanding conditions, cooperators increase in frequency in spatially expanding populations. Fluorescently labeled colonies show genetic demixing of cooperators and defectors, followed by increase in cooperator frequency as cooperator sectors overtake neighboring defector sectors. Together with lattice-based spatial simulations, our results suggest that spatial population expansion drives the evolution of cooperation by (1) increasing positive genetic assortment at population frontiers and (2) selecting for phenotypes maximizing local deme productivity. Spatial expansion thus creates a selective force whereby cooperator-enriched demes overtake neighboring defector-enriched demes in a "survival of the fastest." We conclude that colony growth alone can promote cooperation and prevent defection in microbes. Our results extend to other species with spatially restricted dispersal undergoing range expansion, including pathogens, invasive species, and humans.

A) Populations composed of all cooperators (red) have a higher growth rate than pure defector populations (green), but B) cooperators lose to defectors within mixed populations. Growth rate in A) was assayed on agar plates by measuring colony radius over time, which is directly proportional to rate of cell division S. cerevisiae []. Lines in B) represent cooperator frequency trajectories, measured with FACS, in shaken liquid culture over the course of one week for four different levels of imposed cost (cycloheximide concentrations: 50, 75, 100, and 150nM, from top to bottom and blue to red).

Results of lattice-based spatial simulations of a PD game in a population expanding in one direction (i.e., a linear front[]). A) Example of the endpoint of a two-dimensional simulation (cooperators in red, defectors in green), while B) shows averages over 100–500 iterations, for two-dimensional (black) and one-dimensional (grey) simulations. Each lattice site is a subpopulation growing logistically to size K = 50 in a metapopulation of dimension 1×150 (one-dimensional) or 25×150 (two-dimensional) sites. The vertical axis in B) gives the frequency of cooperators at the population frontier (defined here as a 1×10 or 25×10 area at the furthest edge of the population) after 200 generations. Horizontal dotted line indicates neutral expectation of this value. Simulations initiated with cooperators at 0.10 frequency in a well-mixed (relatedness = 0) homeland of length 10 sites. Two-dimensional expansions (black) select for cooperation, but one-dimensional expansions (grey) cannot. b = 0.5 for solid lines, and dashed lines denote zero social effect (b = 0); note that the horizontal axis has been normalized by b = 0.5. Simulation parameters: W0 = 1, K = 50, m = 0.2.